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DOI: 10.4172/2329-9509.1000170
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ISSN: 2329-9509

Research open access

Predictors Factors of Low Bone Mineral Density in Dental Panoramic

Radiographs
Núbia Priscilla Kleperon Tavares, Ricardo Alves Mesquita, Tânia Mara Pimenta Amara and Cláudia Borges Brasileiro*
Department of Oral Surgery and Pathology, Universidade Federal de Minas Gerais, Brazil
*Corresponding author: Cláudia Borges Brasileiro, Faculty of Dentistry of UFMG, Department of Oral Surgery and Pathology, 6627, Pampulha, 31270- 010, Belo
Horizonte/MG, Brazil, Tel: +55 31 3409-2489; E-mail: cbbrasileiro@gmail.com
Received date: Feb 05, 2016; Accepted date: Feb 29, 2016; Published date: Mar 05, 2016
Copyright: © 2016 Brasileiro CB, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Osteoporosis is a systemic disease that is considered a public health problem since it presents socioeconomic
impacts. The disease results in micro architectural deterioration of bone tissue and decrease of bone mineral density
(BMD) with consequent increase of bone fragility and susceptibility to fractures. Dual energy X-ray absorptiometry
(DXA) is considered the gold standard for BMD evaluation, but investigations about several panoramic radiography
indices have been done in order to seek a predictor of low BMD so that the dentist can play an important role in
screening patients with low BMD and referring them properly for bone densitometry for osteoporosis investigation.
The aim of this paper is to present a review of mandibular radio morphometric indices evaluated in dental panoramic
radiographies and used to recognize patients with low BMD.

Keywords: Panoramic radiography; Bone mineral
Osteoporosis
Introduction
Osteoporosis is a systemic skeletal disease characterized by
deterioration of bone tissue and consequent decrease in bone mineral
density (BMD). The World Health Organization (WHO) considers
osteoporosis as a public health problem due to its prevalence at world's
elderly population and socioeconomic impacts it generates [1]. The
early diagnosis can prevent fractures, consequence of bone fragility.
Many techniques are available to asses BMD, such as single or dual
energy X-ray absorptiometry (SXA / DXA), single or dual photon
absorptiometry (SPA / DPA), quantitative computerized tomography
(QCT) and quantitative ultrasound (QUS) [2,3]. The most widely used
is DXA of femur and lumbar spine and is expresses as a T score.
According to WHO criteria, patients can be classified as normal (T
score ≥-1.0), osteopenia (-1.0>T score>-2.5) and osteoporosis (T score
≤-2.5) [1]. However, unless the patient is subjected to the diagnostic
test, hardly osteoporosis is detected before the fracture occurs, as it
remains asymptomatic. In dentistry, many studies have investigated the
applicability of panoramic radiography in recognizing patients with
bone mass reduction and risk for osteoporosis, allowing the dentist to
refer a patient medical evaluation to present this risk before it suffers a
fracture. Radiography is the complementary exam most requested in
dentistry and specifically the panoramic radiograph is commonly
applied to patients by dentists to assess intra-osseous lesions,
performing extractions or even as a routine dental examination. The
purpose of this article is to present a review of panoramic radiography
as a predictor of low bone mineral density (BMD). The methodology
used in this paper included a search for literature related to panoramic
radiomorphometric indices related to osteoporosis diagnosis
performed on PubMed database from 2010 through November 2015.
The search was conducted in English language and the keywords used
were “bone mineral density and panoramic”. It was found 154 articles
related to the topic and the articles relating to bone mineral density
density; with other diseases, genetic or congenital conditions, patients exposed
to radiation and similar situations were excluded. After exclusion
criteria, a total of 28 articles were included in this review.
Discussion
Most studies that assess the panoramic radiograph as a tool to
predict low BMD evaluated postmenopausal women, especially
because they are a risk group. The low concentration of estrogen is a
factor that increases bone loss, initially in trabecular bone, and after in
cortical bone. Most studies about panoramic radiographic changes
associated with osteoporosis have been focused on measures of jaw
bone mass or morphology. Klemetti et al. [4] was a pioneer to
investigate the correlation between mandibular cortical morphology
and low BMD to predict the risk for osteoporosis. In this study, the
jaws of 365 women of postmenopausal age were evaluated by dental
panoramic radiography and diagnosed for osteoporosis, osteopenia
and regular examination by DXA. The researchers analyzed the
mandibular cortical bilaterally of each patient and the patients were
divided into three groups: class 1 (C1): the endosteal margin of the
mandibular cortical is clear and sharp on both sides; class 2 (C2): the
endosteal margin of the mandibular cortical shows semilunar defects
(lacunar resorption) or appears to form endosteal cortical residues on
one or both sides; and class 3 (C3): the edge of the mandibular cortical
forms dense cortical endosteal residues and this clearly porous. The
changes found in the mandibular cortex correlate with the BMD of
each patient, being indicative of the risk of osteoporosis. The author
points out; however, that is not an accurate diagnosis, only one
predictor for the risk of the disease. The index proposed by Klemetti is
called Klemetti Index (KI) or Mandibular Cortical Index (MCI).
Since Klemetti research, many studies have been developed with the
goal to perform a qualitative analysis of the aspect of the mandible in
dental panoramic radiographs. Renvert et al. [5] evaluated the
mandibular cortex in the panoramic radiographs of 778 individuals
(53% women) in the age of 59-96 years. The researchers observed the
endosteal margin of the mandibular cortical, if it presented, full or

J Osteopor Phys Act Volume 4 • Issue 1 • 1000170

ISSN:2329-9509 JOPA, an open access journal
Citation: Tavares KNP, Mesquita RA, Amara PTM, Brasileiro CB (2016) Predictors Factors of Low Bone Mineral Density in Dental Panoramic
Radiographs. J Osteopor Phys Act 4: 170. doi:10.4172/2329-9509.1000170

Page 2 of 5

image of lacunar resorption and related to BMD previously assessed by mandibular cortical bone Passos et al. [24]
DXA. The results were significant, with relationship between low BMD and the distance
Bhatnagar et al. [9]
and lacunar resorption in mandibular cortical. Similar results were between the mental
foramen and the Gaur et al. [11]
demonstrated by Singh et al. [6]. The authors showed significant mandibular inferior
correlation between MCI and BMD and demonstrated that none of the cortical bone
Mansour et al. [10]
patients with osteoporosis was classified as C1 and there was a Govindraju and Chandra
prevalence of C3 (77,42%). Normal BMD group was associated with [14]
the C1 finding (76,47%). Bajoria et al. [7] found that three of 23 Bajoria et al [7]
showed were classified as C3 and all were elderly females. Valerio et al. Singh et al. [6]
[8] found a statiscally significant difference between the normal and
low BMD groups (osteopenia and osteoporosis) for MCI. Bhatnagar et Gonial Index (GI) Thickness of the cortical Gaur et al. [11]
bone in the area of the
al. [9] also gonial angle
Bajoria et al. [7]]

Antegonial Index (AI) Thickness of the cortical Gaur et al. [11]

Index Index Description Authors
Mandibular Cortical Mandibular cortical Khojastehpour et al. [13]
Index (MCI) or Klemetti morphology that is
Leite et al. [31]
Index (KI) classified as C1, C2 and
C3 Renvert et al. [5]
Bhatnagar et al. [9]
Gaur et al. [11]
Mansour et al. [10]
Valerio et al. [8]
Govindraju and Chandra
[14]
Kim et al. [12]
Bajoria et al. [7]
Singh et al. [6]
Vijay et al. [22]
Pixel Intensity (PI) Grayscale measurement Khojastehpour et al. [13]
Oliveira et al. [15]
Fractal Dimension (FD) Mathematical analysis of Alman et al. [17]
the radiographic image ,
Koh et al. [18]
which evaluates its
density and texture Oliveira et al. [15]
Sindeaux et al. [19]
Mandibular Cortical Thickness of the Damilakis and Vlasiadis
Width (MCW) or Mental mandibular inferior [35]
Index (MI) cortical in the mental
Khojastehpour et al. [13]
foramen region
Leite et al. [31]
Alman et al. [17]
Passos et al. [24]
Bhatnagar et al. [9]
Gaur et al. [11]
Jagelaviciene et al. [30]
Mansour et al. [10]
Valerio et al. [8]
Govindraju and Chandra
[14]
Kim et al. [12]
Nagi et al. [28]
Sindeaux et al. [19]
Bajoria et al. [7]
Vijay et al. [22]
Panoramic Mandibular Ratio between the Damilakis and Vlasiadis
Index (PMI) thickness of the [35]
bone in the area located
Vijay et al. [22]
in front of the gonial
angle Bajoria et al. [7]
Antegonial Depth (AD) Distance along a Vijay et al. [22]
perpendicular line from
the deepest point of
antegonial notch
concavity to the line
parallel to the inferior
cortical border of the
mandible
Gonial Angle (GA) Angle formed by the Geary et al. [36]
intersection of a line
Vijay et al. [22]
traced tangent to the
lower border of the
mandible and another
line tangent to the
posterior border of
ramus and condyle
Antegonial Angle (AA) Angle formed by two Geary et al. [36]
lines traced parallel to
Vijay et al. [22]
the antegonial region
that intersected the
deepest point of the
antegonial notch
Mandibular Angle (MA) Angle formed by one line Shakeell et al. [23]
tangential to the
posterior border of
ramus and the condyle
and another line
tangential to the inferior
most points at the gonial
angle and the inferior
border of the mandible
Mental Posterior Index Obtained 1 cm, 2 cm Valerio et al. [8]
1, 2, 3 (MPI 1, MPI2, and 3 cm posterior to MI,
MPI3) respectively
Table 1: Indexes of the panoramic radiograph evaluated in the studies
about low bone mineral density (PUBMED 2010-2015).
demonstrated a significant correlation between the degree of
mandibular cortical shape erosion and BMD. Panoramic radiograph
showed 96% specificity and 60% sensitivity in osteoporosis evaluation,
indicating that this is an effective tool screening of osteoporosis.
Mansour et al. [10] found significant correlation between MCI and
BMD of the lumbar pines. The patients classified as C3 on the MCI
presented significantly lowest mean BMD, followed by C2 and C1.
Gaur et al. [11] evaluated panoramic radiographies of 40
postmenopausal women and assessed MCI. The results also indicated a
significant relationship between BMD and MCI. For this index, the

J Osteopor Phys Act Volume 4 • Issue 1 • 1000170

ISSN:2329-9509 JOPA, an open access journal
Citation: Tavares KNP, Mesquita RA, Amara PTM, Brasileiro CB (2016) Predictors Factors of Low Bone Mineral Density in Dental Panoramic
Radiographs. J Osteopor Phys Act 4: 170. doi:10.4172/2329-9509.1000170
specificity was 88.88% and sensitivity was 100%. Kim et al. [12]
performed a research with one hundred and ninety-four
postmenopausal women and found that morphological changes of
mandibular inferior cortical bone are associated with BMD
independent of age, height and weight. Khojastehpour et al. [13]
demonstrated a significant correlation between cortical shape of the
mandible and age. The probability of the patients classified as C2 and
C3 increased with age as also demonstrated by Govindraju and
Chandra [14].
In osteoporosis, bone microarchitecture is changed and thus, the
pattern radiographic image is affected. In digital radiography, shape
and structural pattern of trabecular bone can be evaluated by pixel
intensity (PI) and texture, including fractal dimension (FD). PI is a
grayscale measurement, ranging from 0 (black) to 256 (white) in an 8
bit digital image [15]. Kjojastehpour et al. [16] investigated the relation
between mandibular density measurement (gray scale) in panoramic
radiography and BMD of 115 postmenopausal women. Significant
difference in alveolar bone density was found between normal and
osteoporotic group with Spine Bone Mineral Density (SBMD) and
Femoral Bone Mineral Density (FBMD) T-score ≤ - 2.5 and between
normal and osteoporotic patients with FBMD T-score ≤ - 2.5. The
authors suggested that FBMD is more related to mandibular bone
density than SBMD. For fractal analysis, regions of interest (ROI) are
selected and manipulated in digital panoramic using software available
for free, such as NIH’s Image J [17]. Studies reported differences in FD
between normal and osteoporotic patients, but the relation between
mandibular FD and skeletal BMD is not demonstrated in all studies.
Alman et al. [17] used fractal analysis of trabecular bone in dental
panoramic radiographies to asses men and women BMD. The results
indicated that FD is reliable tool to identify low BMD in both men and
women and FD was significantly higher in males than females. Koh et
al. [18] evaluated postmenopausal women and demonstrated that there
was significant difference in the FD values between osteoporotic and
normal patients (FD values decrease in osteoporotic group compared
with normal group). There was a significant difference in the FD values
among different sites of jaw and the lower premolar region was the
most appropriate site of the jaws for evaluating the FD value on
panoramic radiographs. Besides, age was significantly correlated with
the BMD measurements and FD values were not significantly
correlated with the BMD measurements. Oliveira et al. [15] showed
that FD and PI of the mandibular trabecular bone are a promising tool
to identify patients with low BMD. FD and PI values were significantly
different between normal and osteoporotic groups for the right and left
mandibular angle and for the left mandibular body. Sindeaux et al. [19]
performed FD analysis on mandibular trabecular and cortical bone of
133 dental panoramic radiography from men under 60 year and
postmenopausal women. The results showed differences with statistical
significance in FD values on mandibular cortical bone between
patients with normal BMD and with osteoporosis, however, this
difference was not found on the trabecular bone.
In addition to qualitative analysis, quantitative assessment of
panoramic radiography as low BMD predictor has been reported in
several studies based on radiometric index. In iterature, the most
studied index are: Mandibular Cortical Width (MCW), also called
Mental Index (MI), and Panoramic Mandibular Index (PMI). Linear
measurements less studied include Gonial Index (GI), Antegonial
Index (AI) and Antegonial Depth (AD). Angular measurements
including Gonial Angle (GA), Antegonial Angle (AA) and Mandibular
Angle (MA) are also investigated. Most of the studies was performed in
postmenopausal women and evaluated the MCW or MI, described by
J Osteopor Phys Act
ISSN:2329-9509 JOPA, an open access journal
Page 3 of 5
Ledgerton et al. [20], which is the measure thickness of the mandibular
cortical bone at the mental foramen region. A line parallel to the long
axis of the mandible and tangential to the inferior border of the mental
foramen is drawn. A line perpendicular to this tangent intersecting the
inferior border of the mental foramen is drawn, along which
mandibular cortical width is measure [12]. PMI is a
radiomorphometric method which was presented by Benson et al. [21].
PMI is the ratio between the mandibular cortical bone thickness and
the distance from the mental foramen to the lower edge of the
mandible. Measurements greater than or equal to 0.3 mm was
considered normal values. GI is the measurement of the mandibular
cortical thickness measured on the bisectrix of the angle between the
tangent lines to the posterior border of the mandible ramus and the
bottom of the mandible (normal value is higher than 1.2 mm) [7]. AI is
the measurement of the cortical width in the region anterior to the
gonial at a point identified by extending a line of best fit on the anterior
border of mandible (normal value is 3.2 mm). AD is measured as the
distance along a perpendicular line from the deepest point of
antegonial notch concavity to the line parallel to the inferior cortical
border of the mandible. Normal depth is 1.6 mm (±2). GA is measured
by intersection of a line traced tangent to the lower border of the
mandible and another line tangent to the posterior border of ramus
and condyle on each side (normal GA is 128° ± 7). AA is formed by
two lines traced parallel to the antegonial region that intersected the
deepest point of the antegonial notch (normal angle is 163° ± 2) [22].
MA is angle formed by one line tangential to the posterior border of
ramus and the condyle and another line tangential to the inferior most
points at the gonial angle and the inferior border of the mandible [23].
Studies have demonstrated a significant correlation between thin
MCW or MI and low BMD, especially in postmenopausal women. The
mean cortical widths of the osteopenic/osteoporotic groups were lower
than that of the normal group [13,24,25]. Shakeel et al. [23]
demonstrated a positive correlation between MCW and BMD.
Previous studies reported that mandibular cortical width below 3 mm
at the mental foramen region may be considered threshold value when
predicting low spinal and femoral BMD (osteoporosis or osteopenia)
and is a criterion for referring patients for densitometric evaluation
[26,27]. According to Nagi et al. [28], the inferior cortical presented
thinner than 3 mm (threshold to differentiate normal) in panoramic
radiographs of women with low BMD. For Kim et al. [12], the mean
MCW was 2.7 mm for menopausal women, but the optimal cut-off
value of MI for the diagnosis of osteoporosis was 2.22 mm (sensitivity
67.9% and specificity 78.5%). The authors suggested that women with
mandibular cortical thickness less than 2.5 mm should be referred for
osteoporosis evaluation. Passos et al. [24] observed that MCW was
smaller in osteopenia or osteoporosis group (4.5 mm ± 0.9) than
normal group (4.9 mm ± 1.2) and this difference was statistically
significant. Mansour et al [10] showed that when MI cutoff point was
4.5 mm, all patients >4.5 mm were considered normal and the
sensitivity and specificity were 76.9% and 54.1%, respectively.
Maramatsu et al. [29] showed that the mean MCW for osteoporotic
and normal group were 2.2 and 3.9 mm, respectively. When a
threshold of 2.7 mm was applied, the sensitivity and specificity for
identifying osteoporotic patients were 88.5 and 97.3%, respectively.
Jagelaviciene et al. [30] evaluated the relationship between the bone
mineral density in the calcaneus and the MI in panoramic radiography
in postmenopausal women. The results indicated a significant
correlation between calcaneal BMD and MI. Besides, the authors
reported that when the mandibular cortical width is 3 mm or less, a
reduction of BMD in the calcaneus may be predicted. Khojastehpour et
Volume 4 • Issue 1 • 1000170
Citation: Tavares KNP, Mesquita RA, Amara PTM, Brasileiro CB (2016) Predictors Factors of Low Bone Mineral Density in Dental Panoramic
Radiographs. J Osteopor Phys Act 4: 170. doi:10.4172/2329-9509.1000170
al. [13] and Kim et al. [12] showed that age was significantly correlated
with MI. As age increased, MI decreased. Govindraju and Chandra
[14] showed similar results. MI values were significantly smaller in
older females than males of the same age group. Savic and Pavicin
(2014) demonstrated significant correlation between MI and BMD in
the hip but not in the lumbar spine region.
Few studies have evaluated the relationship between BMD and
mandibular cortical thickness in men. Leite et al. [31] demonstrated
that MCW (MI) had a positive correlation with lumbar spine and
femoral neck BMD. Taguchi et al. [32] investigated the relationship
between MCW and calcaneal BMD in men and women aged 40 or
younger. The results revealed that men with an undetected low
calcaneal BMD could be identified by the MCW measured, while
women with an undetected low calcaneal BMD could not be
recognized. In contrast, Alman et al. [17] reported that MCW have
better diagnostic performance for women with low BMD than men.
Sindeaux et al. [19] evaluated the MCW of 133 dental panoramic
radiographs from men aged under 60 years and postmenopausal
women with osteoporosis and normal BMD. The study revealed that
there are significant differences in MCW between women with
osteoporosis and normal BMD, that presents mean values of MCW
significantly higher (4.036 mm ± 0.930) than women with osteoporosis
(2.752 mm ± 0.859 mm). The authors not found significant differences
between mean values of MCW of men with normal BMD (3.982 mm ±
1.251) and osteoporosis (3.434 mm ± 0.839 mm). The mean values of
MCW between men and women were statiscally the same, but higher
values of MCW were found in men with osteoporosis. Bajoria et al. [7]
also demonstrated that MCW values were smaller in women that in
men. Valerio et al. [8] proposed three new indices based on MI: the
mental posterior index 1 (MPI1), mental posterior index 2 (MPI2) and
mental posterior index 3 (MPI3) obtained 1 cm, 2 cm and 3 cm
posterior to MI, respectively. The results revealed statistically
significant difference between osteoporosis group and the normal and
osteopenia groups in all indices evaluated.
The majority of the studies were performed measuring index with a
manual method. Softwares have been developed to detect the
mandibular cortex on dental panoramic radiography and then the
distance of the lower and upper boundaries is measure (cortical
width). Kavitha et al. [33] developed a computer-aided diagnosis
system to continuously measure mandibular inferior cortical width on
dental panoramic radiographs. The sensitivity and specificity of CAD
system in recognizing postmenopausal women with low spinal BMD
was 90% and women with low femoral BMD was 81.8% and 69.2%,
respectively.
Studies that evaluated the correlation between PMI and BMD are
controversial. Singh et al. [6] revealed a significant correlation between
PMI and BMD. About 48% of osteoporotic group presented PMI
scores of < 0,4 and 50% of osteopenic group had a PMI score of
0,4-0,44. Normal patients presented a PMI score >0,44 (49,1%). Savic
and Pavicin [34] found significant correlations between PMI values
and BMD in the hip but not in the lumbar spine region. According to
Govindraju and Chandra [14], significant difference was seen between
females and males for PMI values. Shakeel et al. [23] demonstrated a
positive correlation between PMI and BMD. Bajoria et al. [7]
demonstrated that the mean PMI in younger individuals was 0.69 and
in older individuals it was 0.64. The mean PMI in males was 0.73
whereas in females it was 0.58. The authors also showed that PMI
decreased with age and was smaller in women than in men. In
contrast, some studies have not shown significant results of correlation
J Osteopor Phys Act
ISSN:2329-9509 JOPA, an open access journal
Page 4 of 5
between PMI and BMD. Damilakis and Vlasiadis [35] compared PMI
and MCW and demonstrated that MCW showed the best performance
for the prediction of patients with low BMD compared to PMI. Passos
et al. [24] observed difference statistically significant in MCW between
osteopenia or osteoporosis women and normal women. Similar results
were found by Bhatnagar et al. [9]. The authors demonstrated a
significant correlation between MCW and BMD and no significant
difference was found in PMI. Panoramic radiograph showed 58%
specificity and 73% sensitivity in assessing osteoporosis. Govindraju
and Chandra [14] showed that PMI were higher in patients classified
as C1 and C2 and they gradually decreased in the C3 category.
In a recent study, Vijay et al. [22] evaluated indexes that are not
usually assessed such as, GA, AA, AD, AI, besides the MI and MCI.
The results revealed that AA e AD were significantly greater in normal
patients when compared with low bone mass individuals (osteoporotic
and osteopenic patients). However, AI could diagnose only four of
twenty three patients with osteoporosis, probably due to the
continuous remodeling in the mandibular cortex with age, dental
status and gender. Bajoria et al. [7] demonstrated that AI and GI had
lower values in females when compared to males. Geary et al. [36]
found that GA and AA were not significantly different between normal
and low bone mass patients. Shakeel et al. (2015) showed positive
correlation between AA and Tscore in female patients, but not in males
patients. Savic and Pavicin [34] showed significant correlation between
AI and BMD in the hip but not in the lumbar spine, but GI did not
show statistically significant correlation with BMD in both regions.
Gaur et al. [11] evaluated panoramic radiographies of 40
postmenopausal women and assessed MI, PMI, GI, AI and a
qualitative index, MCI, and showed significant reductions in mean
values in the osteoporotic group compared to normal and osteopenic
groups in MI, PMI and GI. No significant correlation was seen
between AI and low BMD. Ardakani et al. [37] evaluated the cortical
thickness of the mandibular angle of 60 patients (40 females and 20
males). The mean cortex thickness of the mandible angle on the right
and left sides were 0.99 ± 0.34 mm and 0.98 ± 0.3 mm, respectively.
The results indicated that there is no significant relationship between
mandibular angle cortex thickness in osteoporotic patients compared
to patients with a normal BMD, suggesting that this index is not a
suitable tool for screening patients for a low BMD. Shakeel et al. [23]
showed positive correlation between MA and T-score in male patients,
but not in female patients. In Table 1 is listed the indexes of the dental
panoramic radiograph evaluated in the studies about low bone mineral
density according to the search in PubMed database from 2010
through November 2015.
In conclusion, it was verified that visual and morphometric indices
measured in dental panoramic radiography could be considered a
useful tool to predict low BMD and risk of osteoporosis, especially in
postmenopausal female patients. In this way, being an exam routinely
requested in dental offices, the dentists had an important role in
screening patients with low BMD and referring them properly for bone
densitometry for osteoporosis investigation.
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Volume 4 • Issue 1 • 1000170
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Radiographs. J Osteopor Phys Act 4: 170. doi:10.4172/2329-9509.1000170
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Volume 4 • Issue 1 • 1000170